The anatomical basis of sexual dichromatism in non-iridescent ultraviolet-blue structural coloration of feathers

Despite extensive research on the evolution of avian dichromatism, the anatomical bases for differences between the sexes in species with structurally coloured plumage remain largely unknown. Using full‐spectrum spectrometry and transmission electron microscopy, we compared the colour and morphology of rump feathers of male and female eastern bluebirds (Sialia sialis). The ultraviolet (UV)‐blue feather colour in this species is caused by coherent scattering of light within the medullary ‘spongy layer’ of feather barbs. This spongy layer lies beneath a keratin cortex and on top of a layer of melanin granules that surround a hollow central vacuole. Irregularly shaped electron‐dense regions are present within the cortex. Male and female S. sialis differed substantially in their plumage colour and feather structure. A backwards logistic regression predicted sex with 100% accuracy using the colour variables brightness, UV‐violet (UV‐V) chroma and spectral saturation. A second backwards logistical regression predicted sex with 100% accuracy using relative cortex area and size of air spaces. Thus, S. sialis are dimorphic both in colour and in the structures causing this colour. Multiple regression analyses using data pooled from both sexes indicated that multiple features of feather barb structure contributed to colour variation in complex ways. Brightness was negatively related to the relative surface area of cortex in barb cross‐sections. Hue was positively related and UV‐V chroma was negatively related to the distance between scattering elements (i.e. keratin rods and air spaces) in the spongy layer. In contrast, hue was negatively related and UV‐V chroma was positively related to the thickness of the spongy layer. UV‐V chroma was also negatively related to the relative area of electron‐dense regions in the cortex. Spectral saturation was negatively related to the distance between scatterers and the standard error of the size of air spaces. These results suggest that the dimensions of spongy‐layer elements are critical to colour production, but that UV‐blue coloration can also be modified by the cortex and the thickness of the spongy layer. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84 , 259–271.     

Evidence for sexual selection on structural plumage coloration in female eastern bluebirds (Sialia sialis)

Although the function of ornamental traits in males has been the focus of intensive research for decades, expression of such traits in females has received much less study. Eastern bluebirds (Sialia sialis) display structurally based ultraviolet/blue and melanin-based chestnut plumage, and in males this plumage coloration is related to both reproductive success and competitive ability. Compared to males, female bluebirds show a subdued expression of blue and chestnut ornamental coloration, and we used a combination of an aviary nutritional-stress experiment and four years of field data to test the hypothesis that coloration functions as a signal of female quality. First, we tested the effect of food intake on expression of structural and melanin coloration in female eastern bluebirds to determine whether structural or melanin coloration are condition-dependent traits. Females that were given ad libitum access to food displayed more ornamented structural coloration than females on a food-restricted diet, but there was no effect of the experiment on melanin ornamentation. Second, we used field data to assess whether female ornamentation correlated with measures of mate quality and parental effort. The structural coloration of females predicted first egg date, maternal provisioning rates, and measures of reproductive success. These data indicate that structural coloration is dependent on nutritional condition and suggest that sexual selection is acting on structurally based plumage coloration in female eastern bluebirds.     

Confidence of paternity and paternal care by eastern bluebirds

Male birds are often faced with low confidence of paternityin their mates' offspring, raising the question of how paternalcare covaries with confidence of paternity. We tested the hypothesisthat male eastern bluebirds (Sialia sialis) reduce care of nestlingsin response to experimentally decreased confidence of paternity.Actual paternity, as assessed by DNA fingerprinting, had noeffect on male feeding rates, nor did males reduce care whenconfidence of paternity was experimentally decreased. Malesthat had been removed for 2 days while their mate was fertile(experimental group) fed nestlings at absolute rates similarto those of control males. The proportion of feeding trips providedby males was also similar for control and experimental nests.We found no difference in fledging success and nestling growthbetween experimental and control broods. Seven original residentmales were displaced by previously unbanded males. Althoughthese replacement males appeared to feed nestlings at normalrates, the nests attended by replacement males suffered reducedfledging success compared to control and experimental nests.Overall, we found no evidence that males reduce feeding effortwhen confidence of paternity is experimentally decreased. Malesmay tolerate some reduction in confidence of paternity withoutreducing care if paternal care is crucial to nestling survival.Alternatively, males may assess paternity within a brood usingcues other than their ability to guard their fertile mates.     

Reproductive correlates of plumage coloration of female Mountain Bluebirds

Many studies have shown that the plumage coloration of male birds can act as an honest signal of quality, indicating benefits that a female could gain from pairing with a specific male. In some species, females also display ornamental plumage, but less is known about the function and potential adaptive significance of female coloration because most research has focused on male coloration. Male Mountain Bluebirds (Sialia currucoides) display full body, ultraviolet (UV)‐blue plumage, whereas female plumage is more subdued, with blue color focused on the rump, wing, and tail. During the 2011 and 2012 breeding seasons (May–July) near Kamloops, BC, Canada, we examined coloration of the rump and tail of female Mountain Bluebirds to determine if their plumage could act as an indicator of direct reproductive benefits (e.g., enhanced parental care or reproductive success) to potential mates. We found no relationship between female plumage coloration and either provisioning rate or fledging success. However, female coloration varied with age, with after‐second‐year (ASY) females having brighter, more UV‐blue tail feathers than second‐year (SY) females. In addition, ASY females with brighter, more UV‐blue tails had larger clutches. We also observed positive assortative mating by tarsus length. Because previous work with other species suggests that female body size may be a good predictor of breeding success, males could potentially benefit from pairing with larger females. However, reproductive success did not vary with female size in our study. Although our evidence that structural plumage coloration of female Mountain Bluebirds is a signal of direct reproductive benefits for males (e.g., higher reproductive success) is limited, our results (i.e., ASY females with brighter tails than SY females, and ASY females with brighter tails having larger clutches) do suggest the potential for sexual selection to act on female coloration.     

Winter male plumage coloration correlates with breeding status in a cooperative breeding species

The function of colored ornaments is usually related to thesignaling of individual quality in intra- and intersexual interactions.In cooperative breeding species, where only a fraction of themale population access the breeding status and the other fractionhas the option to help breeding pairs, colored traits mightprovide the females with a reliable information on the qualityof potential mate. Males of the cooperative breeding azure-wingedmagpies (Cyanopica cyanus) display conspicuous blue plumagecoloration. Here we explored the role played by structural bluecoloration of males and the probability of becoming a breederor a helper. Birds were trapped during 4 consecutive years,and feather coloration was measured with a spectrometer. Malesthat became breeders had a more brilliant and saturated bluecoloration and showed a more violet hue in the nonbreeding periodcompared with birds that became helpers. Breeding males alsoshowed a seasonal decline in blueness, whereas the color propertiesof helpers were constant throughout the year. Blueness of individualstrapped in the nonbreeding period was positively correlatedwith body size and condition. These findings are consistentwith a scenario in which nonbreeding blue plumage colorationmay function as a signal of individual quality in the azure-wingedmagpie at the pair formation time and add to growing evidencesuggesting that the nonbreeding season appears particularlyimportant in impacting breeding roles in cooperative breedingbirds.     

Variation in melanin pigmentation of a sexually selected plumage trait and its adaptive value in the Common Snipe Gallinago gallinago

There is increasing evidence that melanin‐based plumage coloration correlates with different components of fitness and that it may act as a social or sexual signal of individual quality. We analysed variation in melanin pigmentation in the outermost tail feathers of the Common Snipe Gallinago gallinago. During courtship flights, male Snipe use their outermost tail feathers to generate a drumming sound, which plays a role in territory establishment and mate choice. As the outermost tail feathers are displayed to females during these flights, we predicted that conspicuous variation in their rusty‐brown (pheomelanin‐based) coloration may act as an honest signal of individual quality. To test this prediction, we spectrophotometrically measured brightness (an indicator of total melanin content) and red chroma (an indicator of pheomelanin content) of the outermost tail feathers in 180 juvenile and adult Common Snipe. An age‐related decline in feather brightness was found exclusively in females, suggesting that melanization could have evolved by natural selection to camouflage incubating birds. In both sexes, brightness of the tail feathers was inversely correlated with their structural quality (as measured with mass–length residuals), suggesting that melanization could increase mechanical properties of feathers and, in males, enhance the quality of courtship sonation. Red chroma positively correlated with total plasma protein concentration, supporting our prediction that pheomelanin pigmentation of tail feathers may act as an honest signal of condition. Our study indicated that variation in the melanin‐based coloration of the outermost tail feathers in the Common Snipe could have evolved as a result of several different selection pressures and it emphasizes the complexity of the processes that underlie the evolution of melanin‐based plumage coloration in birds.     

Male share of provisioning is not influenced by actual or apparent loss of paternity in western bluebirds

Approximately 45% of western bluebird (Sialia mexicana) femaleshave some chicks in the nest that are not sired by their socialmates. Extrapair fertilizations account for 42% of offspringin these nests and 19% of nestlings overall. I tested the hypothesisthat males reduce nestling provisioning when their certaintyof paternity or share of paternity is reduced. Capture and detentionof socially monogamous males for 1 h or 24 h during the layingperiod reduced males' copulatory access and their ability tomate guard, increasing the frequency with which extrapair malesintruded and attempted to copulate with resident females. Malesdetained during laying did not reduce their share of feedingtrips compared to control males detained during incubation,compared to unmanipulated males, or compared to males that werecaptured but not detained. Males detained on territory for 1h during the laying period did not reduce their share of feedingtrips when they observed male intrusion, nor when they observedtheir mates accepting extrapair copulations. Males that witnessedtheir mates accepting extrapair copulations did not reduce theirshare of risk in provisioning. Genetic fingerprinting at nonexperimentalnests indicated that males also failed to reduce their feedingcontributions when their estimated share of paternity was reduced,even when a helper male was present to reduce the impact onnestlings. These results suggest that male western bluebirdsdo not make significant adjustments in their share of provisioningwhen they have evidence of partial paternity loss. Togetherwith prior results, this study suggests that western bluebirdmales use an all-or-none rule, contributing approximately halfof the parental provisioning at nests, as long they have somecopulatory access to the female during egg laying.     

Adaptive coloration in pied flycatchers (Ficedula hypoleuca)—The devil is in the detail

Understanding the origin and persistence of phenotypic variation within and among populations is a major goal in evolutionary biology. However, the eagerness to find unadulterated explanatory models in combination with difficulties in publishing replicated studies may lead to severe underestimations of the complexity of selection patterns acting in nature. One striking example is variation in plumage coloration in birds, where the default adaptive explanation often is that brightly colored individuals signal superior quality across environmental conditions and therefore always should be favored by directional mate choice. Here, we review studies on the proximate determination and adaptive function of coloration traits in male pied flycatchers (Ficedula hypoleuca). From numerous studies, we can conclude that the dark male color phenotype is adapted to a typical northern climate and functions as a dominance signal in male–male competition over nesting sites, and that the browner phenotypes are favored by relaxed intraspecific competition with more dominant male collared flycatchers (Ficedula albicollis) in areas where the two species co‐occur. However, the role of avoidance of hybridization in driving character displacement in plumage between these two species may not be as important as initially thought. The direction of female choice on male coloration in pied flycatchers is not simply as opposite in direction in sympatry and allopatry as traditionally expected, but varies also in relation to additional contexts such as climate variation. While some of the heterogeneity in the observed relationships between coloration and fitness probably indicate type 1 errors, we strongly argue that environmental heterogeneity and context‐dependent selection play important roles in explaining plumage color variation in this species, which probably also is the case in many other species studied in less detail.     

The separate effects of egg size and parental quality on the development of ornamental plumage coloration

The fitness‐related consequences of egg size, independent of the influences of parental quality, are poorly understood in altricial birds. Not only can egg size and parental quality influence growth and survival, but each could influence the development of condition‐dependent plumage coloration in offspring. The Eastern Bluebird Sialia sialis is an altricial, multi‐brooded, cavity‐nesting passerine in which juveniles display dichromatic UV‐blue plumage. Previous research suggests that plumage coloration acts as a signal of individual quality among juvenile and adult Eastern Bluebirds. Here, we separate the effects of egg size and parental quality (defined by egg size laid) on nestling growth and plumage ornamentation by exchanging clutches of large eggs with clutches of small eggs. Nestlings were significantly larger immediately post‐hatching when hatched from a large egg, but to maintain a larger size, nestlings needed to have hatched from a large egg and to have been reared by high‐quality parents. Nestlings were brighter when reared by high‐quality parents and this relationship was strongest later in the breeding season. Nestlings exhibited greater UV chroma if hatched early in the season, but UV chroma was not significantly affected by egg size or parental quality. These findings demonstrate varying influences of both egg size and parental quality on offspring growth and plumage ornamentation but suggest that quality of post‐hatching investment is more influential than pre‐hatching investment.     

Haemosporidian parasites depress breeding success and plumage coloration in female barn swallows Hirundo rustica

Parasites are major effectors of natural selection and also play a role in sexual selection processes. Haemosporidian blood parasites are common in vertebrates and have been shown to vary in their effects depending on both the parasite and host species, on the host trait investigated as well as on host condition and stage of infection. Here we investigated infection of adult barn swallows Hirundo rustica by Plasmodium, Leucocytozoon and Haemoproteus species during the chronic stage of infection and the consequences for host fitness traits. Prevalence was higher than 10% only for Plasmodium. Chronic stage infection by Plasmodium was associated with reduced female breeding success, but did not affect breeding dates. Infection did not affect the expression of male secondary sexual traits (tail length and melanin‐based plumage coloration), but was associated with paler coloration of females. Finally, we found a negative effect of infection by Plasmodium on feather growth rate in older but not in yearling individuals. Because feathers are moulted during wintering in sub‐Saharan Africa where infection of barn swallows by Plasmodium occurs, our results suggest that male secondary sexual traits have little potential to reveal acute‐stage infection whereas plumage coloration of females may advertise their infection status. In addition, these results suggest that infection by Plasmodium can influence the course of plumage moult. Thus, our results add to the observations of negative effects of haemosporidian infection on fitness traits in birds and provides evidence that these effects can vary among traits and in relation to age and sex.     

Red coloration and male parental behaviour in the threespine stickleback

In an anadromous population of the threespine stickleback, male red coloration was correlated with agonistic and egg care behaviour of parental males, but not with hatching success. When one male took over a neighbour's territory, the dominant male had more intense red coloration.     

Variation in effects of male plumage ornaments: the case of Iberian Pied Flycatchers

It has been proposed that mate preferences by female Pied Flycatchers Ficedula hypoleuca differ between southern (Iberian) and northern (Scandinavian) European populations. Whereas the size of the white forehead patch, but not plumage colour, has been reported to be a sexually selected trait in the former, only plumage darkness apparently acts as an ornament in the latter. In addition, northern male Pied Flycatchers become darker with age, a trend not detected until the present study in southern birds. Here we show that in an Iberian population of Pied Flycatchers breeding only a few tens of kilometres from previously studied populations, plumage darkness is associated with mating success and increases with age, whereas the size of the white forehead patch is not related to mating success and is only weakly correlated with age, trends similar to those reported for Scandinavian rather than other Iberian Pied Flycatcher populations. This represents a case of variation in sexually selected traits between geographically close populations of Pied Flycatchers that cannot be explained by sympatry with closely related species. It is proposed that differences in the identity and abundance of environmental stressors may be the cause of this regional variation in sexually selected traits.     

Decoupling of reproductive rates and parental expenditure in a polyandrous butterfly

Current theory postulates that the operational sex ratio (OSR)determines the relative degree of mating competition in thetwo sexes and is in turn influenced by a sexual difference inthe potential reproductive rate (PRR) denned as 1/time out,where time out is the time an individual must spend recoveringfrom a bout of mating activity and/or caring for offspring.In bushcricket mating systems where males provide females witha nuptial gift, relative energy expenditure in offspring influencesthe PRR of males and females and underlies a diet-mediated shiftin the OSR. Here we investigated if there is a similar positiverelationship between relative parental nutrient expenditurein offspring and PRR in the polyandrous butterfly Pieris napi,where female fecundity is strongly dependent on male nuptialgifts at mating. By varying the amount of nutrients femalesreceive at mating and relating this to number of offspring produced,we show that male P. napi have, on average, a nutrient expenditurein offspring equaling that of females. In spite of this, themale reproductive rate is 8–13 times higher than thatof females. Hence the relative degree of parental expenditurein offspring is largely decoupled from the degree of matingcompetition in P. napi. Two alternative explanations are advancedto account for the difference between the butterfly and thebushcricket mating systems.     

Structurally based plumage coloration is an honest signal of quality in male blue grosbeaks

We investigated the signaling function of blue plumage in maleblue grosbeaks (Guiraca caerulea) to determine if structurallybased coloration may act as a reliable signal of quality toconspecifics. Blue plumage results from the microstructureof feather barbules rather than from pigment granules, andthus it is possible that structurally based plumage ornamentsmay function differently from sexually selected ornamental coloration that is pigment based. The plumage of male blue grosbeaksreflects maximally in the blue-ultraviolet range, so most variationin plumage coloration among males is invisible to human observers.In previous research, we showed that increased area of blueplumage on the body is associated with a shift in the wavelengthof maximum feather reflectance toward the ultraviolet and withhigh intensity of light reflected at that maximum, and thatextreme expression of the male ornament is condition dependent.These observations suggest that blue plumage may be an honestadvertisement of male quality. We tested this hypothesis ina wild population of blue grosbeaks. We quantified male qualityin three broad categories. (1) Physical condition was assessed from subcutaneous fat deposits, ectoparasite load, and bodysize. (2) Territory quality was assessed from territory area,prey abundance, and predation risk. (3) Paternal investmentwas assessed from male feeding rate. We found that the bluestmales have the largest body size, maintain the largest territorieswith the greatest prey abundance, and feed nestlings in thefirst nest of the season at the highest rates. We conclude that structurally based plumage coloration functions as an honest,intraspecific signal of quality.     

Achromatic plumage reflectance predicts reproductive success in male black-capped chickadees

The size of achromatic (black, white, gray) plumage patchesserves as a male status signal in many species of birds, butvariation in the colors of these patches has received littleattention. We assessed the relation between achromatic plumagereflectance, dominance rank, body condition, and reproductivesuccess in male black-capped chickadees, Poecile atricapillus.We measured plumage reflectance for five body regions of 40male chickadees in late winter and monitored these males throughoutthe following breeding season to determine whether they survivedto breed, whether they successfully paired, whether their partnerlaid eggs, and both their apparent and realized reproductivesuccess. As expected from past studies, a male's dominance ranksignificantly predicted whether his partner laid eggs. However,only achromatic plumage reflectance significantly predictedother measures of male reproductive performance. Among maleswho fledged at least one offspring, both the brightness of whiteplumage regions and the UV-chroma of melanin-based plumage regionswere significant predictors of the proportion of within-pairyoung in their nests. When we consider all males we measured,assigning zero values to males who failed to sire any offspring,the UV-chroma of melanin-based plumage regions was a significantpredictor of realized reproductive success. Bib size was alsorelated to male realized reproductive success. Our findingssuggest that individual variation in achromatic plumage mayplay an important role in sexual signaling in chickadees.     

Nature versus nurture: Structural equation modeling indicates that parental care does not mitigate consequences of poor environmental conditions in Eastern Bluebirds (Sialia sialis)

How organisms respond to variation in environmental conditions and whether behavioral responses can mitigate negative consequences on growth, condition, and other fitness measures are critical to our ability to conserve populations in changing environments. Offspring development is affected by environmental conditions and parental care behavior. When adverse environmental conditions are present, parents may alter behaviors to mitigate the impacts of poor environmental conditions on offspring. We determined whether parental behavior (provisioning rates, attentiveness, and nest temperature) varied in relation to environmental conditions (e.g., food availability and ectoparasites) and whether parental behavior mitigated negative consequences of the environment on their offspring in Eastern Bluebirds (Sialia sialis). We found that offspring on territories with lower food availability had higher hematocrit, and when bird blow flies (Protocalliphora spp.) were present, growth rates were reduced. Parents increased provisioning and nest attendance in response to increased food availability but did not alter behavior in response to parasitism by blow flies. While parents altered behavior in response to resource availability, parents were unable to override the direct effects of negative environmental conditions on offspring growth and hematocrit. Our work highlights the importance of the environment on offspring development and suggests that parents may not be able to sufficiently alter behavior to ameliorate challenging environmental conditions.     

Female mate choice and male red coloration in a natural three-spined stickleback (Gasterosteus aculeatus) population

Under laboratory conditions, female three-spined sticklebacks(Gasterosteus aculeatus L.) show a mating preference for intenselyred-colored males. We verified this female choice in the fieldby observing a freshwater stickleback population in its naturalhabitat. During the egg collection phase, individual courtingmales were localized with the aid of a dummy of a ripe female,caught and photographed under standardized conditions, and released.After males had stopped collecting eggs, we counted the numberof eggs in the nests. The more intense a male's red breedingcoloration, the more eggs he received. Simultaneous female choiceexperiments in the laboratory suggested that ripe females ofthis population preferred redder males. Breeding activitiesof the males in the field were clustered and seem to be synchronizedwithin clusters. At one of the breeding sites, more intensered males were in better physical condition, but this was notthe case at another site. Although several synchronized breedingcycles were observed, the majority of males seem to completeonly one breeding cycle.